J. Nannoplankton Res. 32 (2), 2012, pp71-74 © 2012 International Nannoplankton AssociationISSN 1210-8049 Printed by Harcourt Colour Print, Swansea

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A transitional Emiliania huxleyi morphotype
Jorijntje Henderiks

Department of Earth Sciences, Uppsala University, Villavägen 16, 75 236 Uppsala, Sweden – email: jorijntje.henderiks@geo.uu.se

Amos WinterDepartment of Marine Sciences, University of Puerto Rico, Mayaguez, PR 00681-9000, Puerto Rico
Manuscript Received 05th May, 2011; Manuscript Accepted 09th March, 2012.

Abstract We recently published on the succession of two distinct morphotypes of Emiliania huxleyi (one heavily

calcified, one more delicate form) during active upwelling offshore of Namibia (Henderiks et al., 2012). Here, we
describe a distinct morphotype (Type T, described herein) of E. huxleyi, which represents a transitional form between
Type A and Type R. This morphotype is characterized by short and thick I-shaped distal shield elements and heavily
calcified inner tube elements that extend irregularly into the central area.
Some coccospheres that showed coccoliths with merged I-elements can be considered an end-member form very
closely resembling E. huxleyi Type R and Reticulofenestra spp. Type T dominated the phytoplankton community inmature upwelled waters offshore Namibia, immediately succeeding coastal-upwelling induced diatom blooms. Type T
was encountered in a relatively restricted geographic area and may therefore provide a qualitative test of the reproductive isolation and/or phenotypic plasticity within natural populations of E. huxleyi morphotypes.

1. The ABC of morphotypes
The cosmopolitan coccolithophore species, Emiliania
huxleyi (Lohmann) Hay and Mohler, inhabits tropicalto polar waters, covering a wide range of oceanographicconditions (e.g. Brand, 1994; Cubillos et al. 2007). Its
distribution is supported by high genetic diversity (Medlin et al. 1996; Iglesias-Rodriguez et al. 2006), as well
as a high degree of morphological variability within andamong natural populations (e.g. Hagino et al., 2005; Hagino and Okada, 2006; Cubillos et al., 2007). Six different morphotypes of E. huxleyi have been described basedon different shape, size and degree of calcification of thecoccoliths (Type A, B, B/C, C, R; Young et al., 2003, andreferences therein and Type O; Hagino et al. 2011).
Young and Westbroek (1991) were the first to confirm
genotypic variation between two different morphotypes(Type A and B) by testing immunological cross-reactions
between the coccolith associated polysaccharide (CAP)of each type and antibodies to the CAP. Schroeder etal. (2005) identified a genetic marker for distinguishingstrains of E. huxleyi Type A from strains of Type B. Morerecently, Cook et al. (2011) provided evidence for photosynthetic pigment and genetic differences between two
main morphotypes found in the Southern Ocean, Type A
and Type B/C. DNA sequencing of plastid gene tufA distinguished morphotypes A, B/C (indistinguishable fromB), and R, while little variation was observed within morphotypes (Cook et al., 2011). Minor, but consistent differences in mitochondrial (cox1b-atp4) gene sequences
appear to be linked to the biogeography and temperature preference/tolerance (ecotypes) of different E. huxleyi strains (Hagino et al., 2011). The two phylogenetic
groups identified by these authors are both dominated byType A strains (28 out of 39 tested), and therefore seem
unrelated to coccolith morphology, despite tight sub-clustering of other tested morphotypes within the clades (3strains of Type R and 4 strains of Type O, respectively).
However, Hagino et al. (2011) did not classify Type A
strains by degree of calcification, which is known to vary

between strains and to remain stable in culture, and which
is suggestive of distinct calcification physiologies within
this common morphotype.
It remains unknown whether different phenotypes andgenotypes can occur within interbreeding populations, orwhether different morphotypes represent reproductively
isolated species. In culture, monoclonal strains (i.e. single genotypes) have never been reported to change fromone morphotype to another, despite experimental evidence for significant phenotypic plasticity (i.e. a phenotypic change of a single genotype in response to changing
environmental conditions) (Paasche, 2002; Langer et al.
2009). No reports of cross-breeding experiments exist– probably because it is not easy to induce the haploidstage within monoclonal diploid strains and other practical complications. However, the identification of "transitional" morphotypes in natural populations may provide
qualitative evidence for the viability and/or frequency of
cross-breeding between different morphotypes.
2. The succession of morphotypes
Two distinct morphotypes of E. huxleyi were found tobe part of the phytoplankton succession during coastal
upwelling offshore of Namibia (Henderiks et al., 2012).
Plankton sampling during cruise 48/5 of the R/V Meteor
in October 2000 (Alheit, 2000; Figure 1) revealed that aheavily calcified E. huxleyi morphotype, herein describedas Type T (but labeled as Type A* in Henderiks et al.,2012; Plate 1d), was the dominant coccolithophore in mature upwelled waters immediately after exhaustion of diatom blooms that were found closer to shore. Type T occurred in high abundance with up to >1 million cells l-1 atwater depths between 0-50m. The highest cell concentrations were encountered at station 579, where they caused
a chlorophyll and 19'-hexanoyloxyfucoxanthin maximum
at ~17m depth. At the same time, a more delicate E. huxleyi morphotype (Type B/C; Plate 1a) dominated further
offshore, in very late-succession stage upwelling and oceanic waters (Henderiks et al., 2012). Here, we provide

72Henderiks Winterelement (Plate 1d,e) is a very consistent feature in the sampled populations.
Young (1994) argued that such features
are due to secondary dissolution of thecentral tube, and part of a spectrum fromlightly etched to 'collapsed' coccoliths.
No data on in situ pH were available forthis study (see also discussion in Henderiks et al., 2012), but it is interesting
to note that the heavily calcified E. huxleyi morphotypes discovered in low-pH
upwelling waters offshore Chile did notshow such supposedly 'etched' features(Beaufort et al., 2008; 2011).
We also note that, despite obvious
differences in coccolith size and coccosphere diameter (compare Plate 1g),
the CA of Type T is very similar to theCA of Reticulofenestra parvula var. tecticentrum (Okada & McIntyre 1977)
Jordan & Young, 1990, an overcalcified
form of Reticulofenestra in which theinner tube cycle closes the central area,
Figure 1: Stations sampled during Cruise 48/5 of the R/V Meteor, October 2000. Black symwithouta central collar between the CAbols: Emiliania huxleyi populations (see Plate 1). Grey symbols: no coccolithophores.
and distal shield elements.
Based on its irregular grill structure
additional photographic evidence for the observed morphological variation of E. huxleyi offshore Namibia (Plate in the CA, its heavily calcified, but short and incomplete
distal shield elements, as well as size (<4µm), we con1) and describe Type T.
clude that E. huxleyi Type T is a transitional form on a
3. Emiliania huxleyi Type T
morphological spectrum between Type A and Type R
Coccoliths are medium sized (mean size 2.6-3.1 µm; (compare classification in Hagino et al. (2011); their Tarange 2-4 µm), with variable coccosphere diameters ble 1). Unfortunately, no cells were isolated and kept in(mean diameter 4.9 µm; range 3.4-8.4 µm). The dis- culture, so we have not been able to test the phenotypic
tal shield elements are thick and short, with incomplete stability of this form. However, the morphological fea"hammer-head" terminations that we call "I"-elements, as tures of Type T were highly consistent within and between
opposed to the "T"-elements typical for E. huxleyi Type A the sampled populations, while being distinctly different(cf. Young et al., 2003; Plate 1b). Often the distal shield from the other E. huxleyi morphotypes that were encounI-elements are loosely arranged, because they are discon- tered further offshore and later in the plankton succession
nected from neighboring elements at the outer margin, (Plate 1a-c).
and they rarely extend beyond the proximal shield diameter. The inner tube cycle extends into the central area 4. Concluding remarks(CA) with irregularly shaped elements (similar to E. hux- Over the past two decades, our research community hasleyi Type R; Young et al., 2003), which display variable collected extensive evidence for distinct morphotypes,
degree of calcification, maximum thickness at the inner ecotypes and genotypes of E. huxleyi, in the quest to uncycle and irregularly cover the CA, which has not been derstand why this cosmopolitan taxon has a competitive
described for Type R (cf. Young et al., 2003; but see a re- edge over most other coccolithophores. Even if the relacent illustration of a heavily calcified Type R in Beaufort tionship morphotype - ecotype - genotype is not necessaret al., 2011). Type T also differs from Type R in that its ily a straightforward one (e.g. Langer et al., 2009; Hagino
distal shield elements are not as thick to appear merged et al., 2011), it is very important to differentiate ("split")
together (but see rarely encountered 'combination' cocco- between morphotypes in natural samples, test strains forspheres that challenge this distinction; Plate 1e).
morphological stability/plasticity in the laboratory, andType T coccoliths from offshore Namibia do not have further develop a classification scheme that includes tranthe same smooth, over-calcified appearance of morpho- sitional forms between already established morphotypes.
types observed in the upwelling region offshore Chile(Beaufort et al., 2008; 2011), the heavily calcified forms Referencesthat have been observed in the Bay of Biscaye under sum- Alheit, J. 2000. METEOR-Berichte 06-5, Cruise 48, Leg5, Walvis Bay - Walvis Bay, October 13- October 30,mer conditions (Beaufort & Heussner, 2001) or Type A
2000,
www.dfg-ozean.de/fileadmin/DFG/Berichte/"overcalcified" cf. Young et al. 2003. Instead, the presence
Report_M48_5KS_.pdf.
of a gap between the distal shield elements and inner tube

A transitional Emiliania huxleyi morphotype73

Plate 1
Scanning electron micrographs of Emiliania huxleyi morphotypes encountered offshore Namibia(cruise 48/5 of the R/V Meteor in October 2000). Scale bars: (a-e) = 2 µm, (f) = 1 µm.

a.
b.
c.
d.
e.
f.

Type B/C coccosphere with double layer of coccoliths. Station 536 (surface).
Type A coccosphere, rarely encountered in our samples. Station 536 (surface).
'over-calcified' Type A, nearly entirely covered central area, found to co-exist with Type B/C. Station 536 (surface).
Type T coccosphere with double layering of coccoliths. Station 579 (chlorophyll maximum).
Type T-R coccosphere, transitional form, merged distal shield elements (Type R-like) on some coccoliths, others as described for Type T, withshort and thick I-elements. None of the distal elements connected by central collar. Station 578 (surface).
Reticulofenestra parvula var. tecticentrum, as illustrated in Young et al., 2003 (image credits M. Geisen & J. Young). Inner tube cycle closing
the CA irregularly, distal shield elements not connected by central collar. However, note scale bar = 1 µm; coccoliths and coccosphere diameterof this specimen are significantly smaller than the illustrated E. huxleyi morphotypes.

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